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Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa

An important prelude to bacterial infection is the ability of a pathogen to survive independently of the host and to withstand environmental stress. The compatible solute trehalose has previously been connected with diverse abiotic stress tolerances, particularly osmotic shock. In this study, we com...

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Autores principales: Woodcock, Stuart D., Syson, Karl, Little, Richard H., Ward, Danny, Sifouna, Despoina, Brown, James K. M., Bornemann, Stephen, Malone, Jacob G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8084333/
https://www.ncbi.nlm.nih.gov/pubmed/33872310
http://dx.doi.org/10.1371/journal.pgen.1009524
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author Woodcock, Stuart D.
Syson, Karl
Little, Richard H.
Ward, Danny
Sifouna, Despoina
Brown, James K. M.
Bornemann, Stephen
Malone, Jacob G.
author_facet Woodcock, Stuart D.
Syson, Karl
Little, Richard H.
Ward, Danny
Sifouna, Despoina
Brown, James K. M.
Bornemann, Stephen
Malone, Jacob G.
author_sort Woodcock, Stuart D.
collection PubMed
description An important prelude to bacterial infection is the ability of a pathogen to survive independently of the host and to withstand environmental stress. The compatible solute trehalose has previously been connected with diverse abiotic stress tolerances, particularly osmotic shock. In this study, we combine molecular biology and biochemistry to dissect the trehalose metabolic network in the opportunistic human pathogen Pseudomonas aeruginosa PAO1 and define its role in abiotic stress protection. We show that trehalose metabolism in PAO1 is integrated with the biosynthesis of branched α-glucan (glycogen), with mutants in either biosynthetic pathway significantly compromised for survival on abiotic surfaces. While both trehalose and α-glucan are important for abiotic stress tolerance, we show they counter distinct stresses. Trehalose is important for the PAO1 osmotic stress response, with trehalose synthesis mutants displaying severely compromised growth in elevated salt conditions. However, trehalose does not contribute directly to the PAO1 desiccation response. Rather, desiccation tolerance is mediated directly by GlgE-derived α-glucan, with deletion of the glgE synthase gene compromising PAO1 survival in low humidity but having little effect on osmotic sensitivity. Desiccation tolerance is independent of trehalose concentration, marking a clear distinction between the roles of these two molecules in mediating responses to abiotic stress.
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spelling pubmed-80843332021-05-06 Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa Woodcock, Stuart D. Syson, Karl Little, Richard H. Ward, Danny Sifouna, Despoina Brown, James K. M. Bornemann, Stephen Malone, Jacob G. PLoS Genet Research Article An important prelude to bacterial infection is the ability of a pathogen to survive independently of the host and to withstand environmental stress. The compatible solute trehalose has previously been connected with diverse abiotic stress tolerances, particularly osmotic shock. In this study, we combine molecular biology and biochemistry to dissect the trehalose metabolic network in the opportunistic human pathogen Pseudomonas aeruginosa PAO1 and define its role in abiotic stress protection. We show that trehalose metabolism in PAO1 is integrated with the biosynthesis of branched α-glucan (glycogen), with mutants in either biosynthetic pathway significantly compromised for survival on abiotic surfaces. While both trehalose and α-glucan are important for abiotic stress tolerance, we show they counter distinct stresses. Trehalose is important for the PAO1 osmotic stress response, with trehalose synthesis mutants displaying severely compromised growth in elevated salt conditions. However, trehalose does not contribute directly to the PAO1 desiccation response. Rather, desiccation tolerance is mediated directly by GlgE-derived α-glucan, with deletion of the glgE synthase gene compromising PAO1 survival in low humidity but having little effect on osmotic sensitivity. Desiccation tolerance is independent of trehalose concentration, marking a clear distinction between the roles of these two molecules in mediating responses to abiotic stress. Public Library of Science 2021-04-19 /pmc/articles/PMC8084333/ /pubmed/33872310 http://dx.doi.org/10.1371/journal.pgen.1009524 Text en © 2021 Woodcock et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Woodcock, Stuart D.
Syson, Karl
Little, Richard H.
Ward, Danny
Sifouna, Despoina
Brown, James K. M.
Bornemann, Stephen
Malone, Jacob G.
Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa
title Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa
title_full Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa
title_fullStr Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa
title_full_unstemmed Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa
title_short Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa
title_sort trehalose and α-glucan mediate distinct abiotic stress responses in pseudomonas aeruginosa
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8084333/
https://www.ncbi.nlm.nih.gov/pubmed/33872310
http://dx.doi.org/10.1371/journal.pgen.1009524
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